The Genus Nipponopius Fischer (Hymenoptera, Braconidae, Opiinae) New for China, with Description of a New Species

JHR 57: 123–134 (2017) Nipponopius from China 123 doi: 10.3897/jhr.57.11766 RESEARCH ARTICLE http://jhr.pensoft.net

The genus Nipponopius Fischer (Hymenoptera, Braconidae, Opiinae) new for China, with description of a new species

Tong Zhou1, Cornelis van Achterberg1, Zi-Sheng Guo1

1 Shaanxi Key Laboratory for Animal Conservation / Key Laboratory of Resource Biology and Biotechnology in Western China, College of Life Sciences, Northwest University, 229 North Taibai Road, Xi’an, Shaanxi 710069, China

Corresponding author: Zi-Sheng Guo ([email protected])

Academic editor: G. Broad | Received 11 January 2017 | Accepted 18 April 2017 | Published 30 June 2017

http://zoobank.org/C55DE47E-92C0-489D-9E7C-7FF93B7D55B0

Citation: Zhou T, van Achterberg C, Guo Z-S (2017) The genus Nipponopius Fischer (Hymenoptera, Braconidae, Opiinae) new for China, with description of a new species. Journal of Hymenoptera Research 57: 123–134. https://doi. org/10.3897/jhr.57.11766

Abstract Nipponopius glabricaudatus sp. n. from Shaanxi and Ningxia (NW China) is described and illustrated (Hymenoptera: Braconidae: Opiinae). A key to the species of Nipponopius Fischer, 1963, is added and for the first time the male is described and illustrated. The genus is reported for the second time from outside Japan and is new for China. The position of Nipponopius Fischer is discussed and it is accepted as a valid genus.

Keywords Braconidae, Opiinae, Nipponopius, new species, Palaearctic, China, Shaanxi, Ningxia, Japan

Introduction

Nipponopius Fischer, 1963, belongs to the large subfamily Opiinae (Hymenoptera, Bra- conidae), with 2,063 valid species in 39 genera according to Yu et al. (2016). It is a common group containing generally small (2–5 mm) parasitoid wasps, but Nippono- pius Fischer is rarely collected. Opiinae occur worldwide and the world fauna has been reviewed by Fischer (1972, 1977, 1986, 1987). Wharton (1988, 1997), van Achterberg

Copyright Tong Zhou et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 124 Tong Zhou et al. / Journal of Hymenoptera Research 57: 123–134 (2017)

(1997, 2004a, 2004b), van Achterberg and Salvo (1997), van Achterberg and Chen (2004) and Tan et al. (2016) published updates or some additions for the existing keys to the genera of the Opiinae, but the number of genera and the limits of several genera remain still a matter of discussion. Wharton (1997) synonymised the monotypic genus Nipponopius Fischer with Utetes Foerster, 1863, because both share the curved basal carinula at the inner side of the hind tibia. We disagree with including all opine species with this character into one large genus Utetes Foerster s.l. The resulting group is too diverse and provisional DNA data show that probably several lineages are involved (Li et al. 2013). The morphology of Nipponopius Fischer differs distinctly from that ofUtetes Foerster s.s.; best exempli- fied by the morphology of the hind leg, the position of the dorsope of the first metasomal tergite and the incised female hypopygium. Therefore, we concur with Tobias (2000) that Nipponopius Fischer should be treated as a separate genus. Nipponopius can be recognised from all other opiines by the aberrant legs of both sexes (hind coxa ventrally angularly produced (Figs 9, 19, 20), the second-fourth tarsal segments very robust (Figs 8, 15, 17, 18), the telotarsi enlarged (Figs 8, 15, 17) but less so in males (Fig. 18) and the deeply incised hypopygium of females (Figs 13, 14, 17). Nothing is known about the biology of Nipponopius species, but all Opiinae are solitary koinobiont endoparasitoids of larvae of cyclorraphous Diptera. The oviposi- tion may take place in the egg of the host (ovo-larval parasitoid) or in an early instar larva. The parasitoid larva has it final development when the host larva made its puparium and the adult emerges from this puparium. Opiinae may play an important role in the control of dipterous pests as fruit-infesting Tephritidae and mining Agromyzidae.

Material and methods

The specimens were collected by using a sweep net and directly killed and preserved in 70% alcohol. The specimens were chemically treated with a mixture of xylene + alcohol 96% and amyl acetate, respectively (AXA-method; van Achterberg 2009; van Achterberg et al. 2010). For identification of the subfamily Opiinae, see van Achter- berg (1990, 1993), for identification of Nipponopius Fischer, see Fischer (1972) and the diagnosis in this paper, for references to the Opiinae, see Yu et al. (2016) and for the terminology used in this paper, see van Achterberg (1988, 1993). Measurements are taken as indicated by van Achterberg (1988): for the length and the width of a body part the maximum length and width is taken, unless otherwise indicated. The length of the mesosoma is measured from the anterior border of the mesoscutum till the apex of the propodeum and of the first tergite from the posterior border of the adductor till the medio-posterior margin of the tergite. Observations and descriptions were made with an Olympus SZX11 stereomicroscope and fluorescent lamps. Photographic images were made with the Keyence VHX-5000 digital microscope. The examined specimens are deposited in the American Entomological Institute, Gainesville, USA (AEI) and in the College of Life Sciences, Northwest University, Xi’an, China (NWUX). Nipponopius from China 125

Systematics

Nipponopius Fischer, 1963 Figures 1–41

Nipponopius Fischer, 1963: 283, 1972b: 481; Tobias, 1998: 563. Type species (by monotypy): Nipponopius incisus Fischer, 1963 [examined].

Diagnosis. Hind tibia with basal carinula (Fig. 41); mandible triangular with two subequal teeth and hardly twisted, without or a weak ventral carina (Figs 10, 26, 36); apex of antenna with distinct spine (Figs 16, 30, 40); mesopleuron with one groove (= precoxal sulcus) and sternaulus absent (Figs 5, 22, 32); postpectal carina absent; vein CU1b of fore wing as long as vein 3-CU1 (Fig. 1) or somewhat shorter (Figs 17, 31); first subdiscal cell of fore wing distinctly widened apically; vein m-cu of fore wing converging to vein 1-M posteriorly and vein 1-M curved (Figs 1, 17, 31); vein 1-SR+M distinctly sinuate; hind coxa submedially angularly produced ventrally (Figs 5, 9, 19, 20); second-fourth tarsal segments of ♀ very robust (Figs 8, 17, 25), but less of ♂ (Figs 18, 35); telotarsi and arolium enlarged (Figs 8, 15, 17, 18); dorsope rather small, removed from lateral margin of first tergite (Figs 7, 23, 34); hypopygium of♀ large, strongly sclerotized parts deeply incised (Figs 13, 14, 25), basally punctate, laterally and apico-medially with membranous parts. Notes. According to Wharton (1997) Nipponopius Fischer is a junior synonym of Utetes Foerster, 1863, because of the possession of the hind tibial carinula. We agree with Tobias (2000) that Nipponopius deserves a separate status, not the least because of the presence of a rather small dorsope removed from the lateral margin of the first tergite (Figs 7, 23, 34), the angularly protruding hind coxa ventrally (Figs 8, 9, 19, 20) and the long vein CU1b of fore wing combined with apically widened first subdiscal cell (Fig. 1), features absent in Utetes Foerster s.s. Biology. Unknown. Distribution. East Palaearctic: Japan, Far East Russia, China. Two species.

Key to species of the genus Nipponopius Fischer

1 Anterior tentorial pits rather large (Figs 26, 36); precoxal sulcus remain far removed from anterior margin of mesopleuron (Figs 22, 32) and remainder of mesopleuron smooth antero-dorsally; ovipositor sheath glabrous apically (Fig. 25); vein CU1b of fore wing shorter than vein 3-CU1 (Figs 21, 31); first metasomal tergite largely smooth (Figs 23, 24, 34)...... N. glabricaudatus sp. n. – Anterior tentorial pits small (Fig. 2); precoxal sulcus reaching anterior margin of mesopleuron (Fig. 5) and mesopleuron partly crenulate antero-dorsally; ovipositor sheath distinctly setose apically (Fig. 5); vein CU1b of fore wing as long as vein 3-CU1 (Fig. 1); first tergite rather finely punctate-rugose (Fig. 7)...... N. incisus Fischer, 1963 126 Tong Zhou et al. / Journal of Hymenoptera Research 57: 123–134 (2017)

Figures 1–16. Nipponopius incisus Fischer, ♀, holotype. 1 wings 2 head anterior 3 head dorsal 4 antenna 5 habitus lateral 6 mesosoma dorsal 7 first metasomal tergite dorsal8 hind leg lateral 9 hind coxa lateral 10 mandible and occipital carina latero-ventral 11 fore tibial spur 12 outer hind claw lateral 13 hypopygium lateral 14 hypopygium ventral 15 hind tarsus dorsal 16 apical segments of antenna. Nipponopius from China 127

Nipponopius glabricaudatus Zhou & van Achterberg, sp. n. http://zoobank.org/0899D6C7-24E8-4206-9B76-148601CF4CE9 Figures 17–41

Type material. Holotype, ♀ (NWUX), “NW. China: Ningxia, Jingyuan, Mt. Liupan, Erlonghe For[estry] Farm, 23°24'N 106°20'E, c. 1800 m, 2.viii.2015, Jiangli Tan”. Paratype: 1 ♂ (NWUX), “NW. China: Shaanxi, Ningshan, Mt. Qin, Xunyangba, 33°33'N, 108°32'E, c. 1300 m, vii.2014, Jiangli Tan”. Diagnosis. Very similar to the only other known species, N. incisus Fischer, but differs especially by the large anterior tentorial pits, the reduced precoxal sulcus, the shorter vein CU1b of fore wing and the apically glabrous ovipositor sheath. Description. Holotype, ♀, length of body 3.1 mm; of fore wing 4.0 mm. Head. Head slightly transverse, width 1.8 times its median length in dorsal view and temple directly narrowed behind eyes (Fig. 27); antenna with 40 segments, 1.1 times as long as fore wing, third segment 1.3 times as long as fourth segment, length of third, fourth and penultimate segments 1.7, 1.5 and 1.8 times their width, respectively (Figs 29, 30); maxillary palp as long as height of head; labial palp segments slender; occipital carina far separated from hypostomal carina and carina dorsally absent; hypostomal carina wide, protruding (Fig. 28); length of eye in dorsal view 2.7 times temple; temple and vertex sparsely punctate and with long setae; stemmaticum weakly convex, with small depression behind stemmaticum; OOL: diameter of ocellus: POL = 28:10:11; frons distinctly depressed behind antennal sockets, glabrous medially, finely punctate and setose laterally; face punctate, medially elevated (Figs 26, 27), extending as a median carina to level of posterior margin of antennal sockets; width of clypeus 3.0 times its maximum height and 0.6 times width of face; anterior tentorial pits rather large (Fig. 26); clypeus moderately convex, punctate and protruding, ventrally slightly curved and thin; hypoclypeal depression narrow (Figs 26, 28); malar suture largely absent; length of malar space 0.5 times basal width of mandible; mandible triangular and with narrow ventral carina (Fig. 28). Mesosoma. Mesosoma 1.3 times longer than high; dorsal pronope large, elliptical (Fig. 27); pronotal side smooth, only anteriorly and postero-ventrally crenulated (Fig. 22); epicnemial area largely smooth except anterior margin shortly crenulate; precoxal sulcus remain far removed from anterior margin of mesopleuron, moderately wide and distinctly crenulate (Fig. 23); remainder of mesopleuron mostly smooth; episternal scrobe large; pleural sulcus only ventrally finely crenulate (Fig. 22); mesosternal sulcus medium-sized and moderately crenulate, posteriorly smooth; anterior metapleural sulcus crenulate and widened ventrally (Fig. 22), metapleuron largely smooth dorsally, but coarsely reticulate ventrally (Fig. 22); notauli short, crenulated anteriorly and absent posteriorly; medio-posterior depression of mesoscutum long and narrow elliptical; lateral lobes of mesoscutum mostly glabrous, smooth and shiny, with few setae at middle lobe and near notauli; scutellar sulcus deep and with 3 distinct longitudinal carinae, 0.2 times as long as scutellum; scutellum convex, largely smooth except some punctures and with few setae; side of scutellum smooth except some crenulation (Fig. 23); metanotum 128 Tong Zhou et al. / Journal of Hymenoptera Research 57: 123–134 (2017)

Figures 17–20. Nipponopius glabricaudatus sp. n., ♀, holotype, but 18 and 20 of ♂, paratype. 17, 18 habitus lateral 19, 20 hind coxa lateral (arrow pointing to coxal protuberance). smooth except posterior margin shortly crenulate; dorsal surface of propodeum short, punctate-rugose, and with a short medio-longitudinal carina connected to an irregular transverse carina, its posterior surface largely punctate-reticulate (Fig. 23). Wings. Fore wing: pterostigma elliptical; vein r issued just before middle of ptero stigma (Fig. 21); r:2-SR:3-SR:SR1 = 3:15:21:36; SR1 slightly curved;1-CU1:2-CU1 = 1:6; CU1b shorter than 3-CU1; m-cu postfurcal;1-CU1 hardly widened. Hind wing: M+CU:1-M:1r-m = 21:21:14; cu-a straight (Fig. 21). Nipponopius from China 129

Figures 21–30. Nipponopius glabricaudatus sp. n., ♀, holotype. 21 wings 22 mesosoma lateral 23 meso soma and first metasomal tergite dorsal 24 metasoma dorsal 25 legs and hypopygium antero-ventral 26 head anterior 27 head dorsal 28 head lateral 29 basal antennal segments 30 apical antennal segments. 130 Tong Zhou et al. / Journal of Hymenoptera Research 57: 123–134 (2017)

Figures 31–41. Nipponopius glabricaudatus sp. n., ♂, paratype. 31 wings 32 mesosoma and first metasomal tergite lateral 33 id. dorsal 34 metasoma dorsal 35 legs antero-ventral 36 head anterior 37 head dorsal 38 head lateral 39 basal antennal segments 40 apical antennal segments 41 inner side of hind tibia lateral (arrow pointing to carinula). Nipponopius from China 131

Legs. Hind coxa smooth, with long setae, and distinctly protruding ventro-medially (Figs 19, 25); femora widened (Fig. 25); carinula of hind tibia long, sinuate and area behind it largely glabrous (Fig. 41); tarsal claws medium-sized (Fig. 25); length of femur, tibia and basitarsus of hind leg 2.7, 4.6 and 2.0 times their width, respectively. Metasoma. Length of first metasomal tergite1.1 times its apical width, its surface evenly convex, shiny, largely smooth, with dorsal carinae converging basally and par- allel extending to its posterior half (Figs 23, 24), with laterope large and deep (Fig. 22); second suture obsolescent; second to sixth tergites smooth and sparsely setose posteriorly; combined length of second and third tergites 0.4 times total length of metasoma (Fig. 24); ovipositor sheath glabrous, sheath 0.16 times as long as fore wing and 0.6 times as long as hind tibia (Fig. 25). Colour. Irregularly dark brown or brown; mandible (except dark brown apices), palpi, tegulae and legs yellow; wing membrane subhyaline; veins M+CU1 and C+SC+R of both wings partly pale yellowish. Male. Fore wing length 3.7 mm, body length 4.1 mm (Fig. 18). Antenna with 47 segments; mesosternal sulcus medium-sized and completely crenulated; propodeum strongly sculptured, its dorsal surface areolate and reticulate posteriorly (Figs 33, 34); hind coxa with a relatively small protuberance ventro-medially (Fig. 20); hind femur and tibia less robust, with its length 3.4 times and 6.5 times their width, respectively (Fig. 35); first metasomal tergite distinctly convex, with relatively strong rugae between dorsal carina anteriorly (Figs 33, 34) and laterope deep (Fig. 32); body generally black or blackish brown, but mandible (except dark apices), palpi, tegulae and legs pale yellow (Figs 18, 35). Distribution. China (Ningxia, Shaanxi). Etymology. The name is derived from “glaber” (Latin for “hairless”) and “cauda” (Latin for “tail”), because of the glabrous ovipositor sheath of the holotype.

Nipponopius incisus Fischer, 1963 Figures 1–16

Nipponopius incisus Fischer, 1963: 283, 1972b: 481; Tobias, 1998: 563.

Type material. Holotype, ♀ (AEI), “Kami Kochi, Jap[an], 24.vii.1954, Townes Fam- ily”, “Holotype”, “Nipponopius incisus n. sp., ♀, det. Fischer”, “Type No. 260”, “Nip- ponopius incisus Fischer, Type”. Diagnosis. For the differences see the key to species and the diagnosis of N. glabricaudatus sp. n. Redescription. Holotype, ♀, length of body 4.3 mm; of fore wing 4.8 mm. Head. Temple gradually narrowed behind eyes (Fig. 3); antenna with 41 segments, 1.1 times as long as fore wing, third segment 1.2 times as long as fourth segment, length of third, fourth and penultimate segments 2.2, 1.8 and 1.3 times their width, 132 Tong Zhou et al. / Journal of Hymenoptera Research 57: 123–134 (2017) respectively (Figs 4, 16); maxillary palp as long as height of head; labial palp segments slender; occipital carina far separated from hypostomal carina and carina dorsally absent; hypostomal carina wide, protruding (Figs 5, 10); length of eye in dorsal view 1.4 times temple; temple and vertex sparsely punctate and with long setae; stemmaticum weakly convex, with small depression behind stemmaticum (Fig. 3); OOL: diameter of ocellus: POL = 25:8:10; frons distinctly depressed behind antennal sockets, glabrous medially, punctulate and setose laterally, with two deep pits in front of anterior ocellus (Fig. 3); face punctulate, medially elevated (Fig. 2), extending as a median carina to level of posterior margin of antennal sockets; width of clypeus 4.0 times its maximum height and 0.7 times width of face; anterior tentorial pits small (Fig. 2); cly peus moderately convex, punctate and protruding, ventrally slightly curved and thin; hypoclypeal depression narrow (Fig. 2); malar suture curved, deep and short; length of malar space 0.7 times basal width of mandible; mandible triangular and with narrow ventral carina (Figs 5, 10). Mesosoma 1.3 times longer than high; dorsal pronope absent, except for transverse groove; pronotal side smooth, only oblique groove and posteriorly crenulated (Fig. 5); epicnemial area and mesopleuron dorsally narrowly crenulate; precoxal sulcus reaching anterior margin of mesopleuron, moderately wide and distinctly crenulate (Fig. 5); remainder of mesopleuron mostly smooth; episternal scrobe large; pleural sulcus largely smooth (Fig. 5); anterior metapleural sulcus crenulate and widened ventrally (Fig. 5), metapleuron largely smooth dorsally, except rugosity ventrally (Fig. 5); notauli short, finely crenulated anteriorly and absent posteriorly; medio-posterior depression of mesoscutum long and narrow droplet-shaped; lateral lobes of mesoscutum mostly glabrous, smooth and shiny, with few setae at middle lobe and near notauli; scutellar sulcus deep and with 6 distinct longitudinal carinae, 0.2 times as long as scutellum; scutellum convex, largely smooth and with few setae; side of scutellum smooth except some indistinct crenulation (Fig. 6); metanotum largely smooth but posterior margin narrowly crenulate; dorsal surface of propodeum coarsely reticulate, and without medio-longitudinal or transverse carinae, its posterior surface hardly dif- ferentiated (Fig. 5). Wings. Fore wing: pterostigma elliptical; M+CU1 entirely sclerotized; 1-SR long; r issued just before middle of pterostigma (Fig. 1); r:2-SR:3-SR:SR1 = 3:14:23:41; SR1 straight;1-CU1:2-CU1 = 2:15; CU1b equal to 3-CU1; m-cu postfurcal;1-CU1 hardly widened. Hind wing: M+CU:1-M:1r-m = 21:21:14; cu-a straight (Fig. 1). Legs. Hind coxa smooth, with long setae, and angularly protruding ventro-medially (Figs 8, 9); femora widened; tarsal claws robust basally and slender apically (Fig. 12); length of femur, tibia and basitarsus of hind leg 2.6, 5.6 and 2.0 times their width, respectively. Metasoma. Length of first metasomal tergite1.1 times its apical width, medially strongly convex, shiny, rather finely punctate-rugose, with dorsal carinae only near dorsope, and with laterope deep and elliptical (Fig. 5); second suture obsolescent; second to sixth tergites smooth and their apical half setose; combined length of second and third tergites 0.4 times total length of metasoma (Fig. 5); apical third of ovipositor Nipponopius from China 133 sheath distinctly setose, sheath 0.18 times as long as fore wing and 0.8 times as long as hind tibia (Figs 5, 8). Colour. Black; palpi pale yellowish, mandible (except dark brown apices), clypeus, scapus ventrally, annellus, inner orbits above level of antennal sockets, tegulae largely (humeral plate partly dark brown) and legs yellowish-brown; face, temple, metasoma (except first tergite), pterostigma and veins dark brown; wing membrane subhyaline. Distribution. Japan (Honshu, including garden of Imperial Palace in Tokyo; Konishi and Maetô 2000), Far East Russia (Sakhalin oblast).

Acknowledgements

The second author gratefully acknowledge the kindness of the late Dr Henry K. Townes (AEI, Gainesville) to loan him the holotype of Nipponopius incisus. The research was supported jointly by the National Natural Science Foundation of China (NSFC, No. 31201732, 31572300), and the Northwest University Undergraduate Training Pro- gram for Innovation and Entrepreneurship, China (No. 2017155).

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